ReviewBrain regions with mirror properties: A meta-analysis of 125 human fMRI studies
Highlights
► We performed a meta-analysis based on 125 fMRI studies on brain regions with mirror properties. ► We show that an extensive brain network has been attributed mirror-like properties. ► A core fronto-parietal network is active during observation and execution of actions. ► Additional mirror areas are recruited during tasks that engage non-motor functions.
Introduction
Mirror neurons were originally described as visuomotor neurons that fire both when an action is performed, and when a similar or identical action is passively observed (Rizzolatti and Craighero, 2004). These neurons were first discovered using single-cell recordings in macaque area F5 (di Pellegrino et al., 1992, Gallese et al., 1996, Rizzolatti et al., 1996a) and later in the PF/PFG complex within the inferior parietal cortex (Gallese et al., 2002). Since these original studies there has been an explosion of interest in mirror neurons, both in the scientific literature and the popular media, in part because of their purported role in a diverse range of cognitive functions, from imitation and action understanding to social cognition (Iacoboni, 2005, Iacoboni, 2009, Iacoboni et al., 2005, Fogassi et al., 2005, Keysers et al., 2010, Rizzolatti and Fabbri-Destro, 2008, Rizzolatti and Sinigaglia, 2010). Mirror neurons have also been implicated in a range of neurological and psychiatric disorders, including multiple sclerosis (Rocca et al., 2008), schizophrenia (Arbib and Mundhenk, 2005), autism spectrum disorder (ASD) (Cattaneo et al., 2007, Dapretto et al., 2006, Iacoboni and Dapretto, 2006, Williams, 2008) and alexithymia (Moriguchi et al., 2009). Other investigators have argued that evidence for the existence of human mirror neurons is lacking (Dinstein et al., 2008a, Dinstein et al., 2008b, Jonas et al., 2007, Lingnau et al., 2009, Turella et al., 2009), or have challenged claims for the role of mirror neurons in language function (Johnson-Frey, 2003), action understanding (Hickok, 2009) and imitation (Makuuchi, 2005, Molenberghs et al., 2009).
Immediately following the initial reports of mirror neurons in the macaque brain, investigators sought evidence for an analogous mechanism in humans. Based on early human brain-imaging studies that compared neural activity during perceived and executed actions (Rizzolatti et al., 1996b, Decety et al., 1997, Iacoboni et al., 1999), it was widely assumed that the ventral premotor cortex and the pars opercularis of the posterior inferior frontal gyrus (Brodmann area 44) are human homologues of macaque mirror area F5; and that the rostral inferior parietal lobule (IPL) is the human equivalent of mirror area PF/PFG (Rizzolatti et al., 2001, Rizzolatti, 2005, Rizzolatti and Craighero, 2004). Subsequent investigations have used behavioural approaches, transcranial magnetic stimulation (TMS), electroencephalography (EEG), functional magnetic resonance imaging (fMRI) and human single-cell recordings (Mukamel et al., 2010) to provide further evidence for fronto-parietal mirror neuron regions in humans (for recent reviews see Iacoboni and Dapretto, 2006, Fabbri-Destro and Rizzolatti, 2008, Keysers and Fadiga, 2008, Keysers et al., 2010, Cattaneo and Rizzolatti, 2009, Rizzolatti and Fabbri-Destro, 2010, Rizzolatti and Sinigaglia, 2010). These studies have used a variety of tasks to uncover “mirror activity”. Some have employed action observation and execution tasks, analogous to those used in the original monkey investigations (e.g., Chong et al., 2008, Gazzola and Keysers, 2009, Kilner et al., 2009, Molenberghs et al., 2010). Others have used tasks involving stimuli across a range of modalities, including audition (e.g., Gazzola et al., 2006, Lewis et al., 2005, Tettamanti et al., 2005), somatosensation (e.g., Keysers et al., 2004, Schaefer et al., 2009), vision only (e.g., Molnar-Szakacs et al., 2006, Newman-Norlund et al., 2010); as well as tasks employing stimuli with emotional (affective) content (e.g., Carr et al., 2003, Leslie et al., 2004). This wide variety of approaches in humans has led to an ever-expanding number of brain regions being implicated in mirror mechanism functioning.
The aim of the current investigation was to draw together imaging results from all relevant fMRI studies of the human mirror regions, with the goal of determining the range and extent of brain regions implicated. Based upon the original single-cell findings in monkeys (di Pellegrino et al., 1992, Gallese et al., 1996, Rizzolatti et al., 1996a, Gallese et al., 2002), it might be predicted that the human homologues of macaque areas F5 and PF/PFG – the inferior frontal gyrus and inferior parietal lobule, respectively – should be reliably engaged by tasks designed to elicit mirror neuron activity. On the other hand, it has recently been proposed that mirror activity is widespread in the human brain (e.g., Keysers and Gazzola, 2009, Heyes, 2010). If this is true, it might be predicted that brain regions outside the classically defined mirror network would be engaged, depending on task demands. To address these predictions, we performed a meta-analysis of all human fMRI studies in which the authors attributed their findings to mirror neuron functioning. We used a quantitative meta-analysis technique, known as activation likelihood estimation (ALE; Eickhoff et al., 2009), to investigate which brain regions are most reliably associated with human mirror neuron functions. Contrary to previous ALE studies that focused exclusively on action observation (Caspers et al., 2010), imitation (Caspers et al., 2010, Molenberghs et al., 2009), and the role of the mirror system in action understanding (Van Overwalle and Baetens, 2009), our meta-analysis included all fMRI studies in which significant activations were attributed to the mirror system, regardless of task requirements. We also performed a label-based review to determine the Brodmann areas most consistently associated with mirror neuron regions. In follow-up analyses, we separated studies based on whether they targeted the “classical” (motor) mirror neurons, or instead examined activity during observation of auditory, somatosensory or emotional (affective) stimuli.
Section snippets
Literature selection and exclusion criteria
We searched the Web of Science database (http://apps.isiknowledge.com) using the keywords ‘fMRI’ and ‘mirror system’. As of January 2011, this search revealed 438 published, peer-reviewed papers. The inclusion criteria for our analyses were as follows:
- 1.
Studies that explicitly mentioned the mirror system were included, whereas those that did not were excluded (e.g., the search also uncovered studies about “mirrored” hand movements). Three hundred and thirty (330) of the 438 papers met this
Meta-analysis across all included studies
The ALE meta-analysis of all 125 included studies (supplementary Table 2) revealed 14 significant clusters in total (see Fig. 1, Fig. 6 and Table 1 for details), extending over 9 different Brodmann areas and the cerebellum.
Consistent with previous claims for a “classical” fronto-parietal mirror regions in humans (Rizzolatti et al., 2001), we found evidence for consistent activation in the left and right inferior frontal gyrus, the ventral premotor cortex, and the inferior parietal lobule. The
Discussion
The last 20 years has seen a rapid growth in studies on mirror neurons first described in the macaque by Rizzolatti and his colleagues (di Pellegrino et al., 1992, Gallese et al., 1996). The aim of the current investigation was to draw together all relevant findings from published fMRI studies on human mirror neuron regions, with the goal of determining which areas are most reliably active in tasks designed to tap mirror mechanism functioning.
The most striking outcome of our ALE analyses of 125
Acknowledgements
This work was supported by a Project Grant from the National Health and Medical Research Council of Australia (511148), awarded to RC and JBM and a UQ Postdoctoral Fellowship awarded to PM.
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